Facing the global P crisis and environmental issues arising from the energy- intensive production and the extremely limited efficiency of mineral fertilizers in general, improving fertilizer use efficiency of future crops and cropping systems is an issue of increasing importance. Using plant species adapted to infertile soils with the potential to mobilise sparingly soluble soil nutrients, such as white lupin in intercropping systems, as green manure and also for suppression of pathogens is an approach with a long-lasting history in agriculture, reported already in the ancient cultures of Egypt, China, Greece, Rome and South America mainly based on empirical experience (Tisdale & Nelson, 1975). The scientific investigation of the underlying mechanisms started at the end of the 19th century (Prjanischnikow,
1934). The still ongoing issues as demonstrated by recent studies are improving growth and P uptake by wheat (Triticum aestivum L.) (Cu et al., 2005) and increasing maize yield though inhibition of maize infestation by Striga hermonthica (Weisskopf et al., 2009), when intercropped with white lupin (Lupinus albus L.). However, even in the most sophisticated cropping systems developed in the 1920‟s by Aereboe and von Wrangell or in modern organic farming systems, an adequate P supply to crops remains problematic and is meanwhile associated with a declining status of P fertility in many organic farming soils.
In the recent past, various approaches tried to use the knowledge on the mechanisms of root-induced nutrient mobilisation by root exudation or organic meal chelators, protons or hydrolysing enzymes for the development of transgenic plants overexpressing genes mediating the production or the release of the respective root exudates. While in case of Al-detoxification by root-induced malate exudation or release of Fe-mobilising phytosiderophores, impressive results even on the field scale have been achieved (Takahashi et al., 2001; Delhaize et al., 2004), these approaches were largely unsuccessful and not reproducible in case of root-induced P
mobilisation (Koyama et al., 2000; López-Bucio et al., 2000; Delhaize et al. 2001; George et al., 2004). This may be attributed to the fact that the
amount of mobilising root exudates required for sufficient mobilisation of the macronutrient P in the rhizosphere is much higher than for the micronutrient mobilisation or metal detoxification (Neumann & Römheld, 2007). In the most efficient plant species, such as Lupinus albus, the molecular basis of the release mechanism is still unclear and it needs to be established whether MATE transporters or ALMT-like transporters, both highly expressed in mature (MA) clusters with the highest secretory activity (Chapter I), are mediating the release of citrate into the rhizosphere as one of the most efficient carboxylates for P mobilisation in soils (Neumann & Römheld, 2007). Moreover, in a model calculation based on exudation rates determined for CRs, the amounts of carboxylates required for significant P mobilisation in soils and the morphological characteristics of CRs, Neumann & Römheld (2007) demonstrated that the secretory root surface extension induced by CR morphology seems to be quantitatively much more important for efficient P mobilisation in the rhizosphere than the release rates of carboxylates per unit root length or metabolic alterations (Fig. 1). In CRs of Lupinus albus, it was
demonstrated that a major function of metabolic alterations seems to be the production of root exudates with particularly high efficiency in P mobilisation (e.g., citrate instead of malate, efficient forms of acid phosphatases) (Neumann & Römheld, 2007) or root exudates with protective functions against microbial degradation of P-mobilising root exudates (Weisskopf et al., 2006).
Fig. 1 Impact of cluster root characteristics on accumulation of P mobilising root
exudates in the rhizosphere. Increase compared with normal lateral roots (modified after Neumann & Römheld, 2007).
If CR morphology is a major determinant for successful chemical P mobilisation in soils, one of the most interesting aspects is the question whether development of CR requires unique regulators, exclusively present only in cluster-rooted plant species. The fact that root clustering can also be observed in many other plant species under specific growth conditions, such as localized nutrient supply, exogenous hormone applications (Hinchee & Rost, 1992; Kaska et al., 1999), inoculation with phytohormone-producing soil microorganisms (Kaska et al., 1999; Sukumar et al., 2013), points to the possibility that differences in the quantitative expression of general regulatory factors for root development may be the major determinants of cluster root morphology and function. Accordingly, in the present study no CR- specific regulatory features have been identified (Chapters I-III).
This may indicate that by a favourable combination of common gene expression and hormonal signalling, many crop roots may be able to form the highly complex CR- like structures, thereby improving nutrient acquisition. An impressive example in this direction has been recently published by Jing et al. (2010): comparing broadcast and localised field application of ammonium-based P fertilizers on a highly-buffered calcareous soil (pH 8.0). It was possible to induce root clustering in maize in the vicinity of the nutrient depot. Due to the effect of root clustering, rhizosphere acidification induced by ammonium uptake was intense enough to overcome the buffering capacity of the calcareous soil and to reduce the rhizosphere pH by more than 1.5 units, thereby improving the availability of P and micronutrients such as Fe, Zn and Mn. By contrast, in the variant with broadcast application without formation of root clusters, rhizosphere acidification was not intense enough to overcome the buffering capacity of the soil.
Fig. 2 Root clustering, induced by localised application of ammonium and P fertilizers
with nitrification inhibitors can contribute to rhizosphere acidification of maize on highly buffered soils (modified after Jing et al., 2010).
This example illustrates that CR formation can be an option to improve nutrient acquisition even in non cluster-rooted plant species. Therefore, an improved understanding of internal and external factors necessary for the induction and formation of CR can be a powerful tool to develop breeding targets, biotechnological strategies and management practices with the goal to improve nutrient acquisition efficiency by CR formation in crops. Of course this needs to be
always combined with intelligent fertilization strategies to minimize the risk of nutrient depletion by soil-nutrient mining.